Literature review

July and August, 1997

Raising intact male pigs for meat: Detecting and preventing boar taint

JinLiang Xue, DVM, PhD; Gary D. Dial, DVM, PhD, MBA

JLX: Department of Clinical and Population Sciences, College of Veterinary Medicine, 385 Animal Science/Veterinary Medicine, 1988 Fitch Ave, St. Paul, Minnesota 55108

Copyright (C) 1997 American Association of Swine Practitioners
Also available in PDF format.

Summary

Although there are several advantages to raising intact male pigs instead of castrates, boar taint--an unpleasant odor that emanates from boar fat when it is heated--is a potential problem with rearing boars for pork. Two groups of compounds are considered primarily responsible for boar taint: 16-androstenes (mainly 5[alpha]-androstenone) and skatole. The 16-androstene steroids are largely secreted in the testes and then transported to fat tissues. Skatole is produced in the intestine by bacteria and also stored in fat tissues after absorption. Chemical and sensory tests are commonly used to detect boar taint in pork. Chemical tests typically assess tissue concentrations of the compounds associated with taint. Threshold values are proposed for fat concentrations of androstenone and skatole, 1.0 ppm and 0.25 ppm, respectively. Sensory tests classify boar carcasses into either tainted or untainted categories according to test criteria assessed by human evaluators. Human perception of androstenone is under genetic control. Approximately half of adults are not sensitive to androstenone. Men are less sensitive than women. Human perception of androstenone changes with age and can be induced. Since sensory panels are sensitive, trained, and frequently exposed to taint compounds, prevalence of tainted carcasses detected by the panels is much higher than that detected by consumers. Several methods have been studied to identify and prevent tainted carcasses. Genetic selection, reducing slaughter weight, immunization of boars against gonadotropin releasing-hormone (GnRH), and injection of GnRH agonist have resulted in decreased fat concentrations of androstenone.

Keywords: boars, taint, skatole, androstenone, intact males

Received: September 16, 1996
Accepted: May 24, 1997

Although there are several advantages to rearing entire male pigs for meat,1 the possibility of boar taint--an unpleasant odor that emanates from the fat when the pork is heated--is one potential difficulty with the practice. Entire male pigs can be reared for pork only when tainted carcasses are prevented from entering the fresh meat market. For this article, we review boar taint and its compounds, factors affecting boar taint, and methods to prevent taint.

Chemical causes of boar taint

The smell and/or taste of boar-tainted meat has been described variously as an "off" or "boar" odor;2 onion-like, perspiration-like, or urine-like;3 like perfume, wood, musk, or "Ivory" soap;4 sweet, fruity, ammonia-like, and animal-like;5 and fecal or bitter.6 Williams, et al.,7 found that the odor was sex-dependent. In their study, 36% of intact males possessed the odor, but only 1% of sows, 5% of gilts, and 5% of barrows did. It was not until 1968 that one of the contributory compounds, 5-androst-16-en-3-one (5-androstenone), was isolated and this pork characteristic was labeled "boar taint."8-9

Attempts to identify chemical compounds responsible for boar taint in pork were initiated by Lerche,10 who described the parotid gland as processing the bad odor. Prelog, et al.,11 isolated

  • C19-[Delta]16-steroid,
  • 5[alpha]-androst-16-en-3[alpha]-ol (5[alpha]-androstenol), and
  • 5[alpha]-androst-16-en-3[beta]-ol (5[beta]-androstenol),

and described them as possessing a musk-like odor. Their subsequent studies found that

  • ketone,
  • androstadienone, and
  • 5[alpha]-androstenone

possessed urine-like or perspiration-like smells.12

Craig and Pearson13 reported that sex odor in pork is only found in the fatty tissues. Patterson demonstrated that

  • 5[alpha]-androstenone is present in boar fat,8 and
  • 3[alpha]-hydroxy-5[alpha]-androst-16-ene is present in boar salivary glands,14

suggesting that they are responsible for the odor.

Beery, et al.15 confirmed that both the

  • 3-keto, and
  • 3-hydroxy steroids

are involved in the odor.

Furthermore, Thompson, et al.,16 found that

  • other C19[Delta]16 steroids,
  • 5[beta]-androst-16-en-3-one (5[beta]-androstenone), and
  • 5[alpha]- and 5[beta]-androstenols

also contribute to sex odor. Subsequently, 5[alpha]-androstenone, 5[alpha]-, and 5[beta]-androstenols were found in the testes,17,18 fat,4,19,20 submaxillary gland and saliva,14,18 and parotid gland21 of boars.

Although the chemical compounds responsible for boar taint are under study, it is generally considered that 16-androstenes, a group of steroids in which 5-androstenone is a main component, are primarily responsible for boar taint.9,22,23 Skatole (3-methyl-indole), which has an intense fecal odor and bitter taste, also has been implicated in causing boar taint.6

16-androstenes and 5[alpha]-androstenone

Physiology of 16-androstenes

The 16-androstenes are synthesized primarily in Leydig cells of boar testes along with other androgens and estrogens, with lesser contributions from the adrenals.9,24 The 16-androstenes produced in the testes are released into the systemic circulation via the spermatic vein.25,26 Due to their hydrophobic property, circulating 16-androstenes are then transported to fat tissue where they are stored (Figure 1). 22,23 The apparent half-life of fat androstenone ranges from 4-14 days in boars of 100 kg (220 lb) of liveweight.27,28 Androstenone storage in fat is reversible. Castrating mature boars results in a progressive decline in serum and loin fat concentrations of androstenone.27,29,30 Serum androstenone concentrations decline more slowly than does testosterone because of androstenone release from fatty tissue.21

Androstenone and other 16-androstene steroids are probably catabolized in the liver.31,32 In young boars (<=100 kg, 220 lb), androstenone is eliminated mainly through the urine, in the form of 5[beta]-androstenol, and in trace amounts through feces.33 In adult boars, 5[beta]-androstenol and, to a lesser extent, 5[alpha]-androstenol are the only 16-androstenes that are eliminated in urine.26,34,35

The 16-androstenes in the circulatory system also are transported to the salivary glands, where they function as pheromones and sexual attractants during the mating process.9,31 Boar salivary glands contain high concentrations of 5[alpha]-androstenone, 5a-, and 5[beta]-androstenols.14 When a mature boar is aroused by the presence of an estrous female or an unfamiliar boar, he champs copious amounts of frothy saliva. This excessive salivation provides a medium for the release of large amounts of 16-androstenes into the environment. These odorous steroids, in particular, 5[alpha]-androstenol and 5[alpha]-androstenone, act as signaling pheromones and trigger the mating stance in the estrous female, or indicate to the other boar that his status is being challenged.36,37 Exposing prepubertal gilts to these pheromones also advances the onset of puberty.38

These compounds also contribute to dominance hierarchies in the agonistic behaviors of pigs. Aggressive boars have a higher concentration of salivary androstenone than control boars.39 Spraying androstenone around newly regrouped growing pigs reduced fighting.40

Factors influencing 16-androstenes

Genetics

Distinct breed differences in taint compounds and taint were reported. Piétrain boars had higher concentrations of androstenone than Belgian Landrace boars.41 Landrace crossbred boars had higher fat concentrations of androstenone compared to Large White crossbreeds at a liveweight of 105 kg (231 lb).42 Correspondingly, there was a higher proportion of tainted carcasses from Landrace crossbred boars. We found differences in concentrations of fat 16-androstenes among Duroc, Hampshire, Landrace, and Yorkshire breeds.43 The Landrace breed has the lowest average salivary concentrations of 16-androstenes and fat concentrations of androstenone and skatole.

Genetic selection can effectively reduce the presence of taint compounds. Heritability of androstenone is estimated to range between 0.25-0.81 in Danish Landrace44,45 and 0.61-0.87 in Large White boars.46,47 Estimated heritability of boar taint intensity ranged from 0.13-0.54.48,49 The mean concentration of fat androstenone was reduced from 0.53-0.12 ppm after selecting for low androstenone for three generations.50

Genetic selection against androstenone may adversely affect reproductive or growth performance. A single-generation selection for low androstenone resulted in delayed puberty in gilts (14 days), but not in boars.47 Testicular size was reduced by selection for three generations.51 Selection for high or low androstenone concentrations for five generations demonstrated that growth rate was highly correlated with a high-androstenone line in which there was more fat tissue in female carcasses.52

Age or body weight

Age or liveweight are associated with fat androstenone concentrations in young boars. Testicular androstenone is undetectable at birth and then gradually increases with age and body weight. Androstenone increases dramatically in both testes and fat around the age of puberty,18,53 particularly during the 100- to 130-kg (220-287 lb) growth period with a concomitant increase in taint intensity.54 An increase in androstenone with age varies among animals. Some boars do not even exhibit a significant rise in fat androstenone concentrations at puberty.18,50,55,56

It is clear that fat concentrations of androstenone and 16-androstene steroids are low when animals are slaughtered before they reach sexual maturity. In Denmark and other European countries, slaughter weight is commonly under or around 100 kg (220 lb), the weight at which pigs reach puberty. Therefore, skatole might be a primary factor responsible for boar taint.57 Relative to these countries, the slaughter weight of pigs in the United States is considerably heavier. Target market weights in the United States commonly range from 100-132 kg (220-291 lb).58 United States producers receive the top price (lowest sort loss) when pigs are marketed in this weight range. Based upon historical trends, it is unlikely that the target market weight in the United States will decrease in the near future.

Management

The presence of sexually receptive females stimulates a rapid rise in plasma androstenone and testosterone concentrations in boars.59 Boars mixed with gilts during rearing may have elevated concentrations of fat androstenone.55,60 At 80 kg (176 lb) of live weight, androstenone content in backfat is not affected by the social conditions during rearing. Between 80 and 95 kg (176 and 209 lb), the proportion of boars with an increase in androstenone content is greater in boars reared with females.55 Mixed-sex rearing in some instances also increases the intensity of odor in boar fat.61 Therefore, split-sex rearing should be practiced if pigs are intended for slaughter at heavier market weight.

Season

A seasonal pattern of androstenone in fat, blood, and semen of boars has been reported in mature boars.31,62,63 Concentrations of androstenone from October through December are about five-fold higher than those in the rest of the year. Under decreasing daylength or an artificial light program that simulates the approach to winter, increased androstenone concentrations were observed.62

Skatole

Formation and metabolism of skatole

Skatole is produced in the large intestine by microbial breakdown of the amino acid tryptophan originating from dietary or endogenous protein.64,65 The bacteria are from the genus Lactobacillus.66,67

Approximately 87% of the available skatole produced in the intestine is absorbed across the intestinal wall and transported in the blood to the liver, where the majority is degraded. The feces only contain 13% of the total microbial gut production of skatole.68,69 The half-life of skatole in blood is approximately 60 minutes and the half-life in muscles and fat tissue is 11 hours.69 The degraded products are then excreted in the urine.70 The nondegraded skatole is deposited in fat and muscle. High concentrations of skatole in fat tissue can give rise to an unpleasant odor or taste.71 The contribution of indole to the unpleasant odor or taste is lower even though fat concentrations of indole may occasionally exceed those of skatole.72

Factors affecting fat concentrations of skatole

Since skatole is formed primarily from a dietary component in the animal intestine, a number of dietary components have been studied for their effect on skatole production. Although skatole is produced from tryptophan, addition of tryptophan to a normal pig diet does not increase fat skatole concentrations73 or taint intensity.74

Dietary and intestinal skatole concentrations do not influence fat skatole concentrations.75,76 In fact, infusion of skatole into the terminal ileum of pigs does not increase skatole concentrations in subcutaneous fat.77 Diets with high fiber contents stimulate the fermentative process in the hind gut78 and increase daily elimination of skatole and indole in feces.75 Because high-fiber diets cause large fecal bulk, concentrations of skatole in feces are not affected by the fiber content of a diet.75 Diets supplemented with antibiotics or antibiotic feed additives (such as tylosin) do not affect fat concentrations of skatole.75,79

Several studies demonstrated that some dietary ingredients affect fat concentrations of skatole. Yeast slurry from breweries elevates skatole concentrations in the hind gut80 and backfat.73,80 Sugar-beet pulp containing a high concentration of nondigested and nonstarch polysaccharides decreases concentrations of indole and skatole in subcutaneous fat and increases fecal output of skatole and indole.81,82

Fat concentrations of skatole may be reduced by management practices. Appetite feeding elicits a higher concentration of skatole in fat compared with restricted feeding.83 Pigs with free access to water or wet feeding have reduced skatole concentrations in their fat tissue relative to dry feeding systems.84 Pigs at higher stocking rates have higher fat concentrations of skatole than pigs kept clean at a lower stocking rate.85 The influence of stocking rate is more significant in summer than in winter.

Detecting boar taint

Prevalence of boar taint

Prevalence of boar taint is reported to vary from 1%-30% in dif-
ferent studies based on subjective sensory tests by laboratory panels.3,7,43,86,87 In an early United States study of the prevalence of sex odor in pork, 25% of the boars showed at least a trace of sex odor.3 In another study,7 a small proportion of barrows, sows, and gilts had a taint problem. In a recent United States study,87 scores of boar meat for taint were quite low, although odor panel scores were higher for boars (102 kg, 225 lb bodyweight) than barrows (108 kg, 238 lb bodyweight). We found 15% of boars at 100 kg (220 lb) of liveweight to be tainted.43 Taint in sow and gilt carcasses has been postulated to be related to the period of the estrous cycle at the time of slaughter.4 Plasma androstenone concentrations decline in the period preceding estrus, with comparatively low concentrations at estrus and an increase post-estrus.88 Fecal skatole concentrations are low during the estrous period and high during the luteal phase.89

Taint associated with androstenone and skatole

Although androstenone and skatole are the main compounds considered responsible for boar taint, disagreement exists among researchers in different countries. In general, skatole is considered a primary compound for taint in Denmark.90 Androstenone is believed to have a higher contribution than skatole to boar taint in most other countries.57,91,92 Our studies indicate that androstenone is more important than skatole for taint.43,93,94,95

Skatole is formed in all male, female, and castrated pigs. It is still not known why only intact male pigs deposit skatole in fat tissues in amounts that can cause problems with taint. Skatole and androstenone seem to have synergetic effects: unpleasant odor associated with androstenone can be strengthened when high skatole concentrations are found simultaneously. Skatole may be a problem if pigs are slaughtered at a light weight, at which androstenone concentrations are low.

Threshold values for taint compounds

Chemical and sensory tests are widely used to detect boar taint in meat from entire male pigs. Chemical tests typically assess tissue concentrations of the compounds associated with taint. Sensory tests classify boar carcasses into either tainted or untainted categories according to test criteria assessed by human evaluators. The threshold concentrations of taint compounds are typically indicated according to the results of chemical tests.

Threshold values, above which a carcass can be considered to be tainted, are proposed by European researchers for both androstenone and skatole. They are 1.0 ppm for fat androstenone and 0.25 ppm for fat skatole.96 In Denmark, 0.20 ppm of fat skatole was used as a threshold.90 Recently, the Danish have increased the threshold of fat skatole to 0.25 ppm (1997).97 Threshold values for both androstenone and skatole in cooked ham are higher than those in fresh meat due to the volatile property of the compounds.98 They are 1.5 and 0.5 ppm for androstenone and skatole, respectively.99

Sensory test for taint

The threshold concentrations used in chemical analysis are based upon panel sensory test findings. The findings of these panels are potentially influenced by several factors.

  • Human perception of androstenone is under genetic control. Approximately 50% of adults cannot detect the odor of androstenone, even at high concentrations.100 In contrast, approximately 15% of adults detect a subtle odor, but are not offended by it, and may even find it pleasant. The remaining 35% are exquisitely sensitive to androstenone, detecting less than 200 parts per trillion in air.101
  • Human sensitivity to androstenone also is influenced by gender. Women tend to be more sensitive to boar taint than men. Kloek102 investigated 100 men and 100 women for their ability to detect 5[alpha]androstenone and found that 46% of the males were unable to detect this compound, while only 24% of the females could not detect it. In addition, among panelists, females rated the odor higher in intensity than males. Griffiths and Patterson5 had similar results. Analysis of the olfactory responses of 50 men and 50 women to a pure sample of 5[alpha]-androstenone showed that only 7.0% of women were unable to detect the odor compared with 44.3% of men.5
  • Human perception of androstenone changes with age. The threshold for the perception of androstenone tends to increase with age in men but decrease in woman.103
  • Human ability to perceive androstenone can be induced. Ten of 20 initially insensitive subjects became sensitive after systematic exposure to androstenone for 6 weeks.104 Some subjects became sensitive to exposure within 1 week after the initiation of exposure. Laboratory panels are often selected based on their sensitivity to taint compounds. They are then trained to detect odor using relatively low concentrations of compounds. It is likely that the sensory threshold will decrease after repeated exposure to compounds during training and testing.104

Consumers' response to taint

It has been reported that acceptability of boar meat varies greatly between laboratory panels and consumers. A trained sensory panel in a laboratory can easily detect "taint" in heated fat samples because they are sensitive to taint and trained. Also, no masking agents such as spices are used in panel tests. When preparing and eating boar meat in the normal domestic environment, consumers' responses to boar meat may differ from panelists' responses. In a Canadian study,105 a potential problem with boar taint was detected by highly trained sensory panel, but was not perceived by a consumer survey. Cowan and Joseph106 reported that laboratory panels found 58% of boars and 31% of barrows contaminated with taint. Consumers, however, were unable to distinguish between tainted and untainted pork sorted by the panels. In fact, consumers were not even able to identify taint in boar meat that had fat concentrations of androstenone above 2.0 ppm.107

It has also been reported that acceptability of boar meat varies differently among different populations. Several studies of the reaction of consumers to boar meat have been carried out in a number of European countries and Canada. In general, British,108,109 Irish,110 Spanish,111 and Canadian112 consumers are not sensitive to boar taint, Dutch and Swedish consumers are sensitive, and French consumers are most sensitive.110 It should be realized that in the French study, the consumers were not randomly selected and were also informed that the study involved testing for boar meat.

Prevention of boar taint

It is imperative to prevent tainted carcasses from entering the fresh food market. Castration is one of the methods to remove testicular synthesis of 16-androstenes, but it also removes the anabolic effect of androgenic steroids.29,113

Preventing tainted carcasses from entering the fresh food market

To prevent tainted carcasses from entering the fresh food market, they must be identified before they are distributed to food markets. An online screening method in slaughterhouse had been used to detect tainted carcasses related to skatole in all Danish slaughterhouses since September 1993.90

A method for assessing boar taint on the slaughter line must satisfy the following criteria, proposed by Bonneau and Russeil:11

  • It must be easy to perform, because of the large number of carcasses to be assessed.
  • It must provide a result quickly to avoid prolonged storage of carcasses. It is particularly important in United States slaughterhouses, where the speed of the slaughter line is very fast. The equipment installed in Danish slaughterhouse may not be suitable for use in the United States because only 80 carcasses can be tested per hour.90
  • It must be inexpensive; otherwise, the economical benefit from rearing boars would be lost.
  • It must be accurate to avoid consumer complaints.

Preventing the production of tainted carcasses

Immunological techniques

Immunological methods have been studied to solve the problem of boar taint. Immunization against 5[alpha]-androstenone has only been partially successful.115-117 The antibodies bind to 5[alpha]-androstenone and block its biological actions. Meanwhile, the steroid-antibody complex delays the metabolic clearance of the steroid. Consequently, in the immunized pigs the concentration of 5[alpha]-androstenone in the circulation is much higher than in normal animals,115 or is not different between immunized and control animals.117

Anti-C19[Delta]16-steroids reduce mean fat tissue concentrations of the C19[Delta]16-steroids and mean sensory scores for taint intensity.118 However, the results vary dependent on animals. Three of 15 immunized boars (20%) had similar concentrations of 5[alpha]-androstenone to those of untreated control boars.118

Active immunization against gonadotropin releasing-hormone (GnRH) has been attempted to block the formation of the steroids that cause boar taint. Immunization reduces the weight of testes and accessory sex glands.119-121 Immunization against GnRH impairs pituitary and Leydig cell function in boars. Plasma concentrations of luteinizing hormone (LH) and testosterone, pituitary LH content, testicular LH receptor content, testis, and sex accessory organ weights are significantly reduced in GnRH-immunized boars compared with controls.122 Concentrations of fat 5[alpha]-androstenone also are reduced after active immunization against GnRH.120

Chemical castration

Androstenone synthesis can be effectively blocked by injecting young mature boars with a GnRH agonist (leuprolide), a human drug approved by the FDA for use in prostate cancer.93 A single injection of the compound initially stimulates LH and testosterone secretion, and then depresses androgen hormone production in the testis for at least 30 days. All treated animals had fat concentrations of androstenone below the threshold concentrations 1 month after injection. Thus, it is plausible to give an injection late in the growth period to entire males, thus disrupting testicular production of taint androgens and allowing them to be eliminated from the pig's body prior to slaughter.

Meat processing

Androstenone and skatole are volatile and can be evaporated during processing or heating.123 Acceptibility of boar meat from tainted carcasses was improved after processing.98,99,123 The intensity of boar taint was reduced in cooked boar meat.124 It appears that taint can be reduced or eliminated through heating. Developing a precooked product is a feasible method to find a niche market for boar meat.

Other methods

Feeding level is reported to correlate negatively with strength of taint.125 Boars fed ad libitum have higher concentrations of skatole and androstenone in fat83 than their littermates on restricted feed (85%) at 100 kg (220 lb) of liveweight.118 High energy intake stimulates testicular development and androstenone production, and thus, androstenone accumulation in fat.126 Similar results with pigs of 130 kg (287 lb) of slaughter weight (70% restriction) were reported by Brennan, et al.54

Administering growth hormone (GH) by daily injection from 65-105 kg (143-231 lb) liveweight reduces fat androstenone concentrations in boars.127 Administering GH with sustained-release implants for 6 weeks before slaughter at 87 kg (192 lb) (171 days of age) results in reduced concentrations of boar taint in the loinchops from boars as assessed by a trained sensory panel.128 Boars given GH for 18 weeks have improved boar taint scores compared with untreated boars.129

Implications

  • Due to boar taint, male pigs cannot be reared for meat at current slaughter weights in the United States even though there are several advantages to rearing intact males instead of castration.
  • Vaccination of GnRH or injection of the GnRH agonist to intact males may be effective methods to prevent production of tainted animals.
  • If potentially tainted animals can be identified before vaccination or injection, the number of animals to be vaccinated or injected will be significantly reduced.

References

1. Xue JL, Dial GD, Pettigrew J. Performance, carcass, and meat quality advantages of boars over barrows: A literature review. Swine Hlth Prod 1997;5:21-28.

2. Bratzler LJ, Soule RP, Reineke EP, Paul P. The effects of testosterone and castration on the growth and carcass characteristics of swine. J Anim Sci. 1954;13:171-176.

3. Self HL. The problem of pork odor. Proc 9th Am Meat Inst Found Res Conference, University of Chicago, 1957;9:53.

4.Beery KE, Sink JD, Patton S, Ziegler JH. Characterization of the swine sex odor (SSO) components in boar fat volatiles. J Food Sci. 1971;36:1086-1090.

5. Griffiths NM, Patterson RLS. Human olfactory responses to 5[alpha]-androst-16-en-3-one -principal component of boar taint. J Sci Food Agric. 1970;21:4-6.

6. Vold E. Fleischproduktionseigenschaften bei Ebern und Kastraten. IV. Organoleptische und gaschromatografische Untersuchungen Wasserdampfflüchtiger Stooffe des Rückenspeckes von Ebern. Meld Nordlandrukshoegsk. 1970;49:1-25.

7. Williams LD, Pearson AM, Webb NB. Incidence of sex odor in boars, sows, barrows and gilts. J Anim Sci. 1963;22:166-168.

8. Patterson RLS. 5[alpha]-androst-16-ene-3-one: - Compound responsible for taint in boar fat. J Sci Food Agric. 1968;19:31-38.

9. Gower DB. 16-Unsaturated C19 steroids - a review of their chemistry, biochemistry and possible physiological role. J Steroid Biochem. 1972;3:45-103.

10. Lerche H. Geschlechtsgeruch bei eberkastraten. Z Fleisch Milchhyg. 1936;46:417-420.

11. Prelog von V, Ruzicka L, Wieland P. Über die herstellung der beiden moschusartig riechenden [Delta]16-androstenole (3) und verwandter verbindungen. Helvetica Chimica Acta. 1944;27:66-71.

12. Prelog von V, Ruzicka L, Meister P, Wieland P. Untersuchunger über den zusammenhang zwischen konstitution und geruch bei steroiden. Helvetica Chimica Acta. 1945;28:618-627.

13. Craig HB, Pearson AM. Some preliminary studies on sex odor in pork. J Anim Sci. 1959;18:1557(Abstr.).

14. Patterson RLS. Identification of 3[alpha]-hydroxy-5[alpha]-androst-16-ene as the musk odor component of boar submaxillary salivary gland and its relationship to the sex odor taint in pork meat. J Sci Food Agric. 1968;19:434-438.

15. Beery KE, Sink JD, Patton S, Ziegler JH. Characterization of the sex odor components in porcine adipose tissue. J Am Oil Chem Soc. 1969;46:439A(Abstr.).

16. Thompson RH, Pearson AM, Banks KA. Identification of some C19[Delta]16 steroids contributing to sex odor in pork. J Agric Food Chem. 1972;20:185-189.

17. Claus R, Hoffmann B, Karg H. Determination of 5[alpha]-androst-16-en-3-one, a boar taint steroid in pigs, with reference to relationships to testosterone. J Anim Sci. 1971;33:1293-1297.

18. Booth WD. Changes with age in the occurrence of C19 steroids in the testis and submaxillary gland of the boar. J Reprod Fert. 1975;42:459-472.

19. Claus R, Hoffmann B. Determination of [Delta]-16-steroids in boars. Acta Endocr. 1971;155:(Suppl): 70(Abstr.).

20. Beery KE, Sink JD. Isolation and identification of 3[alpha]-hydroxy-5[alpha]-androst-16-en-one from porcine adipose tissue. J Endocr. 1971;51:223-224.

21. Claus R. Mammalian pheromes with special reference to the boar taint steroid and its relationship to other testicular steroids. In Gunther KD & Kirchgessner M (eds). Advances in Animal Physiology and Animal Nutrition. 1979; No.10, Verlag Paul Parey, Hamburg and Berlin.

22. Bonneau M. Compounds responsible for boar taint with special emphasis on androstenone: A review. Livest Prod Sci. 1982;9:687-705.

23. Brooks RI, Pearson AM. Steroid hormone pathways in the pig, with special emphasis on boar odor: A review. J Anim Sci. 1986;62:632-645.

24. Ahmad N, Gower DB. The biosynthesis of some androst-16-enes from C21 and C19 steroids in boar testicular and adrenal tissue. Biochem J. 1968;108:233-241.

25. Gower DB, Harrison FA, Heap RB. The identification of C19-16-unsaturated steroids and estimation of 17-oxosteroids in boar spermatic vein plasma and urine. J Endocr. 1970;47:357-368.

26. Saat YA, Gower DB, Harrison FA, Heap RB. Studies on the biosynthesis in vivo and excretion of 16-unsaturated C19 steroids in the boar. Biochem J. 1972;129:657-663.

27. Claus R. Messung des ebergeruchstoffes im fett von schweinen mittels eines radioimmunotests. 2. Mitteilung: Zeitlicher verlauf des geruchdepotabbaues nach der kastration. Z Tierz Züchtungsbio. 1976; l93:38-47.

28. Bonneau M, Meusy-Dessolle N, Léglise PC, Claus R. Relationships between fat and plasma androstenone and plasma testosterone in fatty and lean young boars during growth and after hCG stimulation. Acta Endocr. 1982;101:119-128.

29. Cliplef RL, Grinwich DL, McKay RM. Levels of 5[alpha]-androst-16-en-3-one (5-androstenone) in serum and fat of intact and castrated mature boars. Can J Anim Sci. 1985;65:247-250.

30. Grinwich DL, Cliplef RL, McKay RM. Measurement of 16-androstenes (5[alpha]-androst-16-en-3- one/5[alpha]-androst-16-en-3[alpha]-ol) in saliva of mature boars of two breeds following castration. Can J Anim Sci. 1988;68:969-972.

31. Claus R. Pheromone bei saugetieren unter besonderer berucksichtigung des ebergeruchsstoffes und seiner beziehung zu anderen hodensteroiden. Z Tierphys Tierern Futtermittelkd. 1979;10:133-136.

32. Fish DE, Cooke GM, Gower DB. Investigation into the sulfoconjugation of 5[alpha]-androst-16-en-3[beta]-ol by porcine liver. FEBS Lett. 1980;117:28-32.

33. Bonneau M, Terqui M. A note on the metabolism of 5-androst-16-en-3-one in the young boar in vivo. Reprod Nutr Dévelop. 1983;23:899-905.

34. Gower DB, Harrisson FA, Heap RB, Patterson RLS. The identification of C19[Delta]16 steroids in boar urine and spermatic vein plasma. J Endocr. 1970;46:xviii-xiv.

35. Gower DB, Harrisson FA, Heap RB, Saat YA. Studies on the in-vivo biosynthesis and excretion of C19[Delta]16-unsaturated steroids in the boar. J Endocr. 1972;52:iii-iv.

36. Melrose DR, Reed HCB, Patterson RLS. Androgen steroids associated with boar odor as an aid to the detection of estrus in pig artificial insemination. Br Vet J. 1971;127:497-502.

37. Perry GC, Patterson RLS, MacFie HJH, Stinson CG. Pig courtship behavior: pheromonal property of androstene steroids in male submaxillary secretion. Anim Prod. 1980;31:191-199.

38. Brooks PH, Cole DJA. The effect of the presence of a boar on the attainment of puberty in gilts. J Reprod Fert. 1970;23:435-440.

39. Booth WD. Endocrine and exocrine factors in the reproductive behavior of the pig. Symposia Zoological Soc of London. 1980;45:289-311.

40. McGlone JJ, Stansbury WF, Tribble LF. Aerosolized 5[alpha]-androst-16-en-3-one reduced agonistic behavior and temporarily improved performance of growing pigs. J Anim Sci. 1986;63:679-684.

41. Bonneau M, Desmoulin B, Dumont BL. Qualités organoleptiques des viandes de porcs mâles entiers ou castrés: composition des graisses et odeurs sexualles chez les races hypermusclées. Ann Zootech. 1979;28:53-72.

42. Házas Z. Carcass quality and fattening performance of boars, barrows and sows, kept under industrial conditions. World Rev Anim Prod. 1986;22:3-11.

43. Xue JL, Dial GD, Holton EE, Vickers Z, Squires EJ, Lou Y, Gobdout D, Morel N. Breed differences in boar taint: Relationship between tissue levels of boar taint compounds and sensory analysis of taint. J Anim Sci. 1996;74:2170-2177.

44. Jonsson P, Andresen Ø. Experience during two generations of within lines boar performance testing, using 5[alpha]-androst-16-ene-3-one (5[alpha]-androstenone) and an olfactory judgement of boar taint. Ann Génét Sél Anim. 1979;11:24--250.

45. Jonsson P, Joergensen JN. Selektion in der schweinezucht unter berücksichtigung des dominanzverhaltens. Archiv Tietzucht. 1989;32:147-154.

46. Bonneau M, Sellier P. Fat androstenone content and development of genital system in young Large White boars: genetic aspects. World Rev Anim Prod. 1986;22:27-30.

47. Sellier P, Bonneau M. Genetic relationships between fat androstenone level in males and development of male and female genital tract in pigs. J Anim Breed Genet. 1988;105:11-20.

48. Wismer-Pedersen J, Jonsson P, Jensen P, Banyai A. The occurrence of sex odor in Danish Landrace pigs. In Rhodes DN (ed), Meat Production from Entire Male Animals, London. 1969;p285-295.

49. Jonsson P, Wismer-Pedersen J. Genetics of sex odor in boars. Livest Prod Sci. 1974;1:53-66.

50. Willeke H, Claus R, Müller E, Pirchner F, Karg H. Selection for high and low level of 5[alpha]-androst-16-en-3-one in boars. I. Direct and correlated response of endocrinological traits. J Anim Breed Genet. 1987;104:64-73.

51. Willeke H, Claus R, Pirchner F, Alsing W. A selection experiment against 5[alpha]-androst-16-ene-3- one, the boar taint steroid, in adipose tissue of boars. Z Tierzuct ZuchtBiol. 1980;97:86-94.

52. Willeke H, Pirchner F. Selection for high and low level of 5-androst-16-en-3-one in boars. II. Correlations between growth traits and 5[alpha]-androstenone. J Anim Breed Genet. 1989;106:312--317.

53. Claus R. Messung des ebergeruchstoffes im fett von schweinen mittels eines radioimmunotests. 1. Mitteilung: Geruchsdepotbildung in abhängigkeit vom alter. Z Tierz Züchtungsbiol. 1975;92:118-126.

54. Brennan JJ, Shand PJ, Fenton M, Nicholls LL, Aherne FX. Androstenone, androstenol and odor intensity in backfat of 100- and 130- kg boars and gilts. Can J Anim Sci. 1986;66:615-624.

55. Bonneau M, Desmoulin B. Evolution de la teneur en androsténone du tissu adipeux dorsal chez la porc mâle entier de type Large White: variation selon les conditions d'élevage. Reprod Nutr Dév. 1980; 20:1429-1437.

56. Bonneau M, Carrie-Lemoine J, Prunier A, Garnier DH, Terqui M. Age-related changes in plasma LH and testosterone concentration profiles and fat 5[alpha]-androstenone content in the young boar. Anim Reprod Sci. 1987;15:241-258.

57. Bonneau M, Denmat ML, Vaudelet JC, Veloso Nunes JR, Mortensen AB, Mortensen HP. Contributions of fat androstenone and skatole to boar taint: I. Sensory attributes of fat and pork meat. Livest Prod Sci. 1992;32:63-80.

58. Roker J, Dial G. Getting the most for your pork in U.S. markets. Proc Am Assoc Swine Prac 26th Ann Meeting, Omaha, Nebraska, Mar 4-7, 1995. p197-209.

59. Narendran R, Etches RJ, Hacker RR, Bowman GH. Effect of sexual stimulation on concentrations of 5[alpha]-androstenone and testosterone in the peripheral plasma of boars reared individually. Anim Reprod Sci. 1982;4:227-235.

60. Patterson RLS, Lightfoot AL. Effect of sex grouping during growth on 5[alpha]-androstenone development in boars at three commercial slaughter weights. Meat Sci. 1984;10:253-263.

61. Walker N. Boars for meat production - the effect of single-sex or mixed-sex groups on growth performance and carcass characteristics. Rec Agric Res North Ire. 1978;26:7-10.

62. Claus R, Schopper D, Wagner H-G. Seasonal effect on steroids in blood plasma and seminal plasma of boars. J Steroid Biochem. 1983;19:725-729.

63. Trudeau VL, Grinwich DL, Sanford LM. Seasonal variation in the blood concentration of 16-androstenes in adult Landrace boars. Can J Anim Sci. 1988;68:565-568.

64. Yokoyama MT, Carlson J R. Microbial metabolites of tryptophan in the intestinal tract with special reference to skatole. Am J Clin Nutr. 1979;32:173-178.

65. Wilkins CK. Analysis of indole and skatole in porcine gut contents. Int J Food Sci Tech. 1990;25:313-317.

66. Chung KT, Anderson GM, Fulk GE. Formation of indoleacetic acid by intestinal anaerobes. J Bacteriol. 1975;124:573-575.

67. Yokoyama MT, Carlson J R, Holdeman LV. Isolation and characteristics of a skatole-producing Lactobacillus sp. from the bovine rumen. Appl Environ Microbiol. 1977;34:837-842.

68. Agergaard N, Laue A. Absorption from the gastrointestinal tract and liver turnover of skatole. In Bonneau M (ed), Measurement and Prevention of Boar Taint in Entire Male Pigs. Paris, France; Institut National de la Recherche Agronornique (INRA). 1993;p107-111.

69. Agergaard N, Laue A. A physiological study of skatole, a major component of boar taint in male pigs. Proc 13th IPS Congr, June 26-30, 1994, Bangkok, Thailand. p495.

70. Friis C. Distribution, metabolic fate and elimination of skatole in the pig. In Bonneau M (ed), Measurement and Prevention of Boar Taint in Entire Male Pigs. Paris, France; Institut National de la Recherche Agronornique (INRA). 1993;p113-115.

71. Lundström K, Hansson, KE, Fjelkner-Modig S, Person J. Skatole - another contributor to boar taint. Proc 26th Eur Meeting of the Meat Res Workers, Colorado Springs, Aug 31-Sept 5, 1980;1: 300-303.

72. Lundström K, Malmfors B, Malmfors G, Petersson H, Stern S, Mortensen AB, Sorensen SE. Boar taint and bitter taste as affected by androstenone and skatole. Proc 30th Eur Meeting of Meat Res Workers, Bristol Sept 9-14, 1984. p379-398.

73. Pedersen JK, Mortensen AB, Madsen A, Mortensen HP, Hyldegaard-Jensen J. [The influence of feed on boar taint in meat from pigs.] National Institute of Animal Science (NIAS), Denmark, Communication, 1986; No. 638: p4.

74. Bonneau M, Desmoulin B. Influence de l'exces de trptophan et des conditions d'elevage sur la frequence des odeurs sexuelles des jeune porcs males entiers: relation avec le developpement de l'appareil genital. J Rech Porc Fr. 1981;13:329-334.

75. Hawe SM, Walker N, Moss BW. The effects of dietary fibre, lactose and antibiotic on the levels of skatole and indole in feces and subcutaneous fat in growing pigs. Anim Prod. 1992;54:413-419.

76. Hawe SM, Walker N. The effects of involuntary coprophagy on production of skatole in growing pigs. Anim Prod. 1991;53:105-109.

77. Hawe SM, Walker N, Moss BW. Effects of infusing skatole into the terminal ileum of growing male pigs. Livest Prod Sci. 1993;33:267-276.

78. Just A, Fernández J, Jorgensen H. The net energy value of diets for growth in pigs in relation to the fermentative processes in the digestive tract and the site of absorption of the nutrients. Livest Prod Sci. 1983;10:171-186.

79. Hansen LL, Larsen AE. Effect of antibiotic feed additives on the level of skatole in fat of male pigs. Livest Prod Sci. 1994;39:269-274.

80. Jensen MT. [Skatole (boar taint). Microbial production of skatole in gastro-intestinal tract of pigs.] National Institute of Animal Science (NIAS), Denmark, Communication,1990; No.772: p2.

81. Gill BP, Hardy B, Perrott JG, Wood JD, Hamilton M. The effect of dietary fiber on the meat eating and fat quality of finishing pigs fed ad libitum. Anim Prod. 1993;56:421-422.

82. Wood DJ, Nute GR, Whittington FM, Kay RM, Perrot JG. Effects of molassed sugar-beet feed on pigmeat quality. Anim Prod. 1994;58:471-472.

83. Øverland M, Berg J, Matre T. The effect of feed and feeding regime on skatole and androstenone levels and on sensory attributes of entire male and female pigs. Prod Util Meat from Entire Male Pigs Milton Keynes, Sept 28-29, 1995.

84. Kjeldsen N. Practical experience with production and slaughter of entire male pigs. In Bonneau M (ed), Measurement and Prevention of Boar Taint in Entire Male Pigs. Paris, France; Institut National de la Recherche Agronornique (INRA). 1993;p137-144.

85. Hansen LL, Larsen AE, Jensen BB, Hansen-Møller J, Barton-Gade P. Influence of stocking rate and temperature on feces deposition in the pen and its consequences on skatole concentration (boar taint) in subcutaneous fat. In Bonneau M (ed), Measurement and Prevention of Boar Taint in Entire Male Pigs. Paris, France; Institut National de la Recherche Agronornique (INRA). 1993; p151-157.

86. Malmfors B, Hansson J. Incidence of boar taint in Swedish Landrace and Yorkshire boars. Livest Prod Sci. 1974;7:411-420.

87. Judge MD, Mills EW, Orcutt MW, Forrest JC, Diekman MA, Harmon BG, Lin RS, Nicholls LL. Utilization of boar meat: Composition, quality and odor incidence in relation to androstenone and skatole. J Anim Sci. 1990;68:1030-1033.

88. Narendran R, Etches RJ, Hacker RR, Bowman GH. 5[alpha]-androstenone concentrations in sow plasma during the estrus cycle. Theriogenology. 1980;13:263-267.

89. Claus R, Bernal-Barragan H, Dehnhard M. Effect of gonadal hormones in mature cyclic sows on food intake and skatole concentrations in feces. J Anim Physiol Anim Nutr. 1991;66:61-68.

90. Armstrong H. Test to track boar taint. Pigs. 1993;9:14-16.

91. Hansson KE, Lundström K, Fjelkner-Modig S, Persson J. The importance of androstenone and skatole for boar taint. Swed J Agric Res. 1980;10:167-173.

92. Malmfors B, Andresen Ø Relationship between boar taint intensity and concentration of 5- androst-16-en-3-one in boar peripheral plasma and back fat. Acta Agric Scand. 1975;25:92-96.

93. Xue JL, Dial GD, Bartsh S, Kerkaert B, Squires EJ, Marsh WE, Ferre G. Influence of a gonadotropin-releasing hormone on circulating concentrations of luteinizing hormone and testosterone and tissue concentrations of compounds associated with boar taint. J Anim Sci. 1994; 72:1290-1298.

94. Xue JL, Dial GD, Schuiteman J, Kramer A, Fisher C, Marsh WE, Morrison RB, Squires JE. Evaluation of growth, carcass, and compound concentrations related to boar taint in boars and barrows. Swine Hlth Prod. 1995;3:155-160.

95. Xue JL, Dial GD, Morrison RB. Comparison of the accuracies of chemical and sensory tests for detecting taint in pork. Livest Prod Sci. 1996;46:203-211.

96. Mortensen AB, Bejerholm C, Pedersen JK. Consumer test of meat from entire males, in relation to skatole in backfat. Proc 32nd European Meeting of Meat Research Workers, Ghent. 1986;p23-26.

97. Bonneau M. Personal Communication. 1997.

98. Bonneau M, Desmoulin B, Frouin A, Bidard JP. Conséquences des processus technologiques de transformation des viandes de porc mâle sur la tenneur en androsténone des graisses. Ann Tech Agric. 1980;29:69-73.

99. Bonneau M, Denmat ML, Vaudelet JC, Veloso Nunes JR, Mortensen AB, Mortensen HP. Contributions of fat androstenone and skatole to boar taint: II. Eating quality of cooked hams. Livest Prod Sci. 1992;32:81-88.

100. Wysocki CJ, Beauchamp GK. Ability to smell androstenone is genetically determined. Proc Natl Acad Sci USA. 1984;81:4899-4902.

101. Amoore JE, Buttery RG. Partition coefficients and comparative olfactometry. Chem Senses Flavor. 1978;3:57-71.

102. Kloek J. The smell of some steroid sex-hormones and their metabolites. Relations and experiments concerning the significance of smell for the mutual relation of the sexes. Psychiat Neurol Neurochir. 1961;64:309-344.

103. Dorries KM, Schmidt HJ, Beauchamp GK, Wysocki CJ. Changes in sensitivity to the odor of androstenone during adolescence. Develop Psychobiol. 1989;22:423-435.

104. Wysocki CJ, Dorries KM, Beauchamp GK. Ability to perceive androstenone can be acquired by ostensibly anosmic people. Proc Natl Acad Sci USA. 1989;86:7976-7978.

105. Sather AP, Squires EJ, Jeremiah LE, Jones SDM, Schaefer AL. Meat quality and consumer acceptance of pork from entire males. Can J Anim Sci. 1992;72:1014-1015.

106. Cowan CA, Joseph RL. Production and quality of boar and castrate bacon. 2. Consumer and panel response to bacon and fat samples. Ir J Food Sci Tech. 1981;15:105-116.

107. Patterson RLS, Elks PK, Lowe DB, Kempster AJ. The effects of different factors on the level of androstenone and skatole in pig fat. Anim Prod. 1990;50:551(Abstr.).

108. Rhodes DN. Consumer testing of bacon from boar and gilt pigs. J Sci Food Agric. 1971;22:485-490.

109. Rhodes DN. Consumer testing of pork from boar and gilt pigs. J Sci Food Agric. 1972;23:1483-1491.

110. Desmoulin B, Bonneau M, Froouin A, Bidard JP. Consumer testing of pork and processed meat from boars: the influence of fat androstenone level. Livest Prod Sci. 1982;9:707-715.

111. Diestre A, Oliver MA, Gispert M, Appa I, Arnau J. Consumer responses to fresh meat and meat products from barrows and boars with different levels of boar taint. Anim Prod. 1990;50:519-530.

112. Cliplef RL, Grinwich DL, Castell AG. Consumer acceptance of fresh pork and pork products from littermate boars and barrows. Can J Anim Sci. 1984;64:21-27.

113. Bonneau M, Meusy-Dessolle N, Leglise PC, Claus R. Relationships between fat and plasma androstenone and plasma testosterone in fatty and lean young boars following castration. Acta Endocr. 1982;101:129-133.

114. Bonneau M, Russeil P. The size of Cowper's (bulbo-urethral) glands as an estimate of boar taint on the slaughter line. Livest Prod Sci. 1985;13:169-178.

115. Shenoy EVB, Daniel MJ, Box PG. The 'boar taint' steroid 5[alpha]-androst-16-en-3-one: An immunization trial. Acta Endocr. 1982;100:131-136.

116. Williamson ED, Patterson RLS. A selective immunization procedure against 5[alpha]-androstenone in boars. Anim Prod. 1982;35:353-360.

117. Williamson ED, Patterson RLS, Buxton ER, Mitchell KG, Partridge IG, Walker N. Immunization against 5[alpha]-androstenone in boars. Livest Prod Sci. 1985;12:251-264.

118. Brooks RI, Pearson AM, Hogberg MG, Pestka JJ, Gray JI. An immunological approach for prevention of boar odor in pork. J Anim Sci. 1986;62:1279-1289.

119. Falvo RE, Chandrashekar V, Arthur RD, Kuenstler AR, Hasson T, Awoniyi C, Schanbacher BD. Effect of active immunization against LHRH or LH in boars: Reproductive consequence and performance traits. J Anim Sci. 1986;63:986-994.

120. Bonneau M, Dufour R, Chouvet C, Roulet C, Meadus W, Squires EJ. The Effects of immunization against luteinizing hormone-releasing hormone on performance, sexual development, and levels of boar taint-related compounds in intact male pigs. J Anim Sci. 1994;72:14-20.

121. Oonk HB, Turkstra JA, Lankhof H, Schaaper WMM, Verheijden JHM, Meloen RH. Testis size after immunocastration as parameter for the absence of boar taint. Livest Prod Sci. 1995;42:63-71.

122. Awoniyi C, Chandrashekar V, Arthur R, Schanbacher BD, Amador A, Falvo RE. Pituitary and Leydig cell function in boars actively immunized against gonadotropin-releasing hormone. J Reprod Fert. 1988;84:295-302.

123. Pearson AM, Ngoddy S, Price JF, Larzelere HE. Panel acceptability of products containing boar meat. J Anim Sci. 1971;33:26-29

124. Chen W, Forrest JC, Peng IC, Pratt DE, Judge MD. Palatability of prerigor cooked boar meat. J Anim Sci. 1993;71:645-650.

125. Elsley FWH, Livingstone RM. Effect of slaughter weight and feeding level on the incidence of boar taint. In: DN Rhodes (Ed.), Meat Production From Entire Male Animals. Churchill, London. 1969;p273-283.

126. Claus R, Weiler U, Herzog A. Physiological aspects of androstenone and skatole formation in the boar - A review with experimental data. Meat Sci. 1994;38:289-305.

127. Bonneau M, Meadus WJ, Squires EJ. Effects of exogenous porcine somatotropin on performance, testicular steroid production and fat levels of boar taint-related compounds in young boars. Can J Anim Sci. 1992;72:537-545.

128. Klindt J, Buonomo FC, Yen JT. Administration of porcine somatotropin by sustained-release implant: Growth, carcass, and sensory responses in crossbred white and genetically lean and obese boars and gilts. J Anim Sci. 1995;73:1372-1339.

129. Klindt J, Buonomo FC, Yen JT, Baile CA. Growth performance, carcass characteristics, and sensory attributes of boars administered porcine somatotropin by sustained-release implant for different lengths of time. J Anim Sci. 1995;73:3585-3595.